Long‐term expanding human airway organoids for disease modeling
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Abstract
Abstract Organoids are self-organizing 3D structures grown from stem cells that recapitulate essential aspects of organ structure and function. Here we describe a method to establish long-term-expanding human airway organoids from broncho-alveolar biopsies or lavage material. The pseudostratified airway organoid epithelium consists of basal cells, functional multi-ciliated cells, mucus-producing goblet cells, and CC10-secreting club cells. Airway organoids derived from cystic fibrosis (CF) patients allow assessment of CFTR function in an organoid swelling assay. Organoid culture conditions also allow gene editing as well as the derivation of various types of lung cancer organoids. Respiratory syncytial virus (RSV) infection recapitulated central disease features and dramatically increases organoid cell motility, found to be driven by the non-structural viral NS2 protein. We conclude that human airway organoids represent versatile models for the in vitro study of hereditary, malignant, and infectious pulmonary disease.
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Infection of murine gastric organoids by H. pylori showed increased cytosolic β-catenin levels induced by bacterially originated CagA, which led to increased proliferation in infected organoids.
“Infection of murine gastric organoids by H. pylori showed increased cytosolic β-catenin levels induced by bacterially originated CagA, which led to increased proliferation in infected organoids179.”
From Organoids (2022) · cites this paper as [179]
The Results section on generation and characterization describes human airway organoids, while the Materials and Methods section describes RSV infection of those organoids; neither addresses murine gastric organoids. Searches for H. pylori, CagA, cytosolic β-catenin, and infection-related proliferation found no passage supporting the attributed finding in our copy. (LLM, conf=0.76)
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Modeling and Targeting Alzheimer’s Disease With Organoids
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Self-citationBeumer, J., Geurts, M. H., Lamers, M. M., Puschhof, J., Zhang, J., van der Vaart, J., Mykytyn, A. Z., Breugem, T. I., Riesebosch, S., Schipper, D., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25729-7 · Cited by 107 · see citing works
Self-citationHaderk, F., Chou, Y., Čech, L., Fernández-Méndez, C., Yu, J. X., Olivas, V. R., Meraz, I. M., Rabago, D. B., Kerr, D. L., Gómez, C. F., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47423-0 · Cited by 106 · see citing works
A pan-cancer organoid platform for precision medicine
Larsen, B. M., Kannan, M., Langer, L. F., Leibowitz, B. D., Bentaieb, A., Cancino, A., Dolgalev, I., Drummond, B. E., Dry, J. R., Ho, C.-S., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109429 · Cited by 105 · see citing works
Advanced 3D imaging and organoid bioprinting for biomedical research and therapeutic applications
Maharjan, S., Ma, C., Singh, B., Kang, H., Orive, G., Yao, J., & Zhang, Y. S. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115237 · Cited by 105 · see citing works
CRISPR engineering in organoids for gene repair and disease modelling
Geurts, M. H., & Clevers, H. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-022-00013-5 · Cited by 103 · see citing works
Self-citationModeling Cell Communication in Cancer With Organoids: Making the Complex Simple
Fiorini, E., Veghini, L., & Corbo, V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00166 · Cited by 103 · see citing works
Human airway cells prevent SARS-CoV-2 multibasic cleavage site cell culture adaptation
Lamers, M. M., Mykytyn, A. Z., Breugem, T. I., Wang, Y., Wu, D. C., Riesebosch, S., van den Doel, P. B., Schipper, D., Bestebroer, T. M., Wu, N. C., et al. (2021) · eLife · doi:10.7554/elife.66815 · Cited by 100 · see citing works
The Use of Stem Cell-Derived Organoids in Disease Modeling: An Update
Azar, J. H., Bahmad, H. F., Daher, D., Moubarak, M. M., Hadadeh, O., Monzer, A., Bitar, S. A., Jamal, M., Al‐Sayegh, M., & Abou-Kheir, W. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147667 · Cited by 100 · see citing works
Organoids: a novel modality in disease modeling
Heydari, Z., Moeinvaziri, F., Agarwal, T., Pooyan, P., Shpichka, A. I., Maiti, T. K., Timashev, P. S., Baharvand, H., & Vosough, M. (2021) · Bio-Design and Manufacturing · doi:10.1007/s42242-021-00150-7 · Cited by 100 · see citing works
Chen, J., Yang, X., Si, H.-R., Gong, Q.-C., Que, T., Li, J., Li, Y., Wu, C., Zhang, W., Chen, Y., et al. (2023) · Cell · doi:10.1016/j.cell.2023.01.019 · Cited by 100 · see citing works
Inhalable Textile Microplastic Fibers Impair Airway Epithelial Differentiation
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Organoids of the female reproductive tract
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- Authors
- Sachs, N., Papaspyropoulos, A., Zomer‐van Ommen, D. D., Heo, I., Böttinger, L., Klay, D., Weeber, F., Huelsz‐Prince, G., Iakobachvili, N., Amatngalim, G. D., de Ligt, J., van Hoeck, A., Proost, N., Viveen, M. C., Lyubimova, A., Teeven, L., Derakhshan, S., Korving, J., Begthel, H., Dekkers, J. F., Kumawat, K., Ramos, E., van Oosterhout, M. F., Offerhaus, G. J., Wiener, D. J., Olimpio, E. P., Dijkstra, K. K., Smit, E. F., van der Linden, M., Jaksani, S., van de Ven, M., Jonkers, J., Rios, A. C., Voest, E. E., van Moorsel, C. H., van der Ent, C. K., Cuppen, E., van Oudenaarden, A., Coenjaerts, F. E., Meyaard, L., Bont, L. J., Peters, P. J., Tans, S. J., van Zon, J. S., Boj, S. F., Vries, R. G., Beekman, J. M., & Clevers, H.
- Affiliations
- University Medical Center Utrecht (NL)
- St. Antonius Ziekenhuis (NL)
- The Netherlands Cancer Institute (NL)
- Institute for Atomic and Molecular Physics (NL)
- Maastricht University (NL)
- Hubrecht Institute for Developmental Biology and Stem Cell Research (NL)
- Princess Máxima Center (NL)
- Royal Netherlands Academy of Arts and Sciences (NL)
- Corresponding author
- Clevers, Hans
- ORCID
- Sachs, Norman
- Papaspyropoulos, Angelos
- Klay, Dymph
- Weeber, Fleur
- Iakobachvili, Nino
- Amatngalim, Gimano D
- de Ligt, Joep
- van Hoeck, Arne
- Proost, Natalie
- Begthel, Harry
- Ramos, Emilio
- Offerhaus, G Johan
- Wiener, Dominique J
- Dijkstra, Krijn K
- Smit, Egbert F
- Jonkers, Jos
- Rios, Anne C
- Voest, Emile E
- Cuppen, Edwin
- Coenjaerts, Frank E
- Meyaard, Linde
- Bont, Louis J
- Peters, Peter J
- Tans, Sander J
- Boj, Sylvia F
- Vries, Robert G
- Beekman, Jeffrey M
- Clevers, Hans
- Venue
- The EMBO Journal
- Published
- 2019-01-14
- Volume
- 38
- Issue
- 4
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC6376275
- OpenAlex
- W2799736418
- Cited by
- 1,082
- References
- 82
- Citations by year
- 2026: 126 · 2025: 178 · 2024: 137 · 2023: 159 · 2022: 157 · 2021: 182 · 2020: 104 · 2019: 30 · 2018: 9
- FWCI
- 86.42
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The EMBO Journal (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, cc-by-nc-nd)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- AMOLF Institutional Repository (AMOLF) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc-nd)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Research Publications (Maastricht University) (submittedVersion, cc-by-nc-nd)
- Utrecht University Repository (Utrecht University) (submittedVersion, cc-by-nc-nd)
- Funders
- ZonMw (114021012, 40‐00812‐98‐14103, 91615182)
- Human Frontier Science Program (CDA00076/2014‐C)
- Prof. Dr. Jaap Swieringa Foundation (stAH‐CvM‐HI‐HC)
- Dutch Cystic Fibrosis Society (HIT‐CF)
- SU2C (SU2C‐AACR‐DT‐12‐14)
- KWF Kankerbestrijding (2014‐7006)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (680‐47‐529, 834.11.002)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Keywords
- airway organoids, cystic fibrosis, CFTR function, lung cancer, metastasis, respiratory syncytial virus, NS2 protein, neutrophil recruitment, disease modeling, Clara cells, ciliated cells
- MeSH terms
- Animals, Carcinoma, Non-Small-Cell Lung, Cells, Cultured, Cystic Fibrosis, Disease Models, Animal, Drug Screening Assays, Antitumor, Epithelial Cells, Female, Humans, Lung Neoplasms, Male, Organ Culture Techniques, Organoids, Respiratory Syncytial Viruses, Respiratory System, Mice, SCID, Mice, Inbred NOD, Respiratory Syncytial Virus Infections, Cystic Fibrosis Transmembrane Conductance Regulator, Xenograft Model Antitumor Assays, Mice
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